J. Exp. Biol. (1965), 43, 581-593
|Si
With 2 plates and 8 text-figures
Printed in Great Britain
THE NERVOUS PATHWAYS FOR POISONING,
EATING AND LEARNING IN OCTOPUS
BY J. Z. YOUNG
Department of Anatomy, University College London
and Stazione Zoologica, Naples
(Received 25 May 1965)
INTRODUCTION
When a strange figure falls in the visual field of an octopus the animal usually
attacks it after a considerable delay. If the attack yields food then on a subsequent
appearance of the figure the attack will be repeated. Within a few trials the octopus
learns to attack the figure regularly and quickly. If conversely no food results, attacks
become slower and soon cease (Young, 1956, 1958). The present work was undertaken to find the pathway by which the signals that teach the animal to attack reach
fr.s.med.
I fr.i.med.
buc.s.
Text-fig. 1. Diagram to show three possible pathways for taste fibres (1) from the lip, (2) from
receptors in the buccal palps or elsewhere in the buccal mass, (3) from the suckers. Also
showing three efferent pathways from the superior buccal lobe: A to the inferior buccal
ganglion, B to the subradular ganglion and C which goes to the posterior salivary glands.
the memory, which is in the optic lobes. There seem to be three possible pathways
(labelled i, 2 and 3 in Text-fig. 1): (1) from the lips that surround the beak, via the
labial nerves and superior buccal lobe; (2) from the receptors in the buccal mass or
farther down the gut, via the sympathetic nerves, inferior buccal ganglia, interbuccal
connectives and superior buccal lobe; (3) from the arms, via the brachial nerves and
582
J. Z. YOUNG
either the cerebro-brachial connective or by a more posterior pathway, the brachiooptic lobe tract (Boycott & Young, unpublished).
The resultant attack might be due to impulses in a combination of these pathways.
It has not been possible to investigate them all equally thoroughly, but evidence will
be given that the learning can take place if the lip has been removed or the labial
nerves severed, but not if the interbuccal connectives have been cut. Pathways from
the arms or lips alone are not therefore able to produce the learned responses.
The details of the connectives of the inferior frontal and superior buccal systems
are considered elsewhere (Young, 1965 a, b). Besides analysing the pathways mentioned above, the present experiments also serve to demonstrate that the bundles
of fibres originating from the back of the superior buccal lobe carry the impulses for
stimulation of the posterior salivary gland secretion which poisons the prey (crabs)
(Ghiretti, i960). Further it is shown that the connectives joining the superior buccal
lobe to the inferior buccal ganglia must be intact if the animal is to open the crab
properly and remove the meat from the skeleton.
The plan of the experiments has been to interrupt the pathways at a series of levels,
from the peripheral nerves in front, backwards through the superior buccal and
posterior buccal lobes.
METHODS
Octopuses were isolated and kept in asbestos tanks 100 x 60 x 40 cm. with circulating sea water and a home of bricks at one end (see Boycott & Young, 1955). Crabs
or white horizontal or vertical rectangles were introduced at the end of the tank
opposite the home and the time taken for the octopus to attack was recorded with a
stop-watch. The food reward for attacking the horizontal rectangle was a small piece
of fish given on the end of a wire. An electric shock (12V. a.c.) was given if the
vertical rectangle was attacked.
Trials were given in sessions in the morning and evening, each session consisting
of five to ten trials, trials being separated by about 5 min. Operations were performed
under urethane anaesthesia (3 % in sea water) and sections were prepared with Cajal's
silver method as previously described.
RESULTS
Removal of the lips
The lip is a ring of tissue, around the beak, surrounded by the arms. It contracts
when touched, even under light anaesthesia, and can only be removed if the animal is
deeply anaesthetized. The operation was performed on seven animals and none
showed any obvious aberrations of behaviour or feeding thereafter. They attacked
crabs seen at a distance and seized, poisoned and ate them apparently like normal
animals.
The attack behaviour of animals was tested at three sessions before and three after
operation by showing crabs, which they were not allowed to eat. The proportion of
attacks was as great after operation as before in several animals, but in a few it fell
slightly giving the means shown in Text-fig. 2.
A white horizontal rectangle was then shown to each octopus and a small piece of
Nervous pathways for poisoning, eating and learning in Octopus
583
fish was given whether or not the object was attacked. The effect of giving food after
the first trial increased the probability of attack at the next one, as in normal animals
(Young, 1956). All the animals came out several times during the first sessions of
eight trials and several continued to attack regularly thereafter (Text-fig. 2). In the
animal of Text-fig. 3 a further extension of the experiment was to show the animal
a vertical rectangle and to give shocks when this was attacked. Food continued to
be given at alternate trials when the horizontal rectangle was shown. Attacks on the
latter at first decreased sharply but by the fifth session the discrimination was made
accurately.
It is concluded that the lip is not essential for the promotion and maintenance of
attacks at an unfamiliar visual figure.
Lip removed
Lip removed
8
7
6
5
J3
s4
< 3
2
< 3
1
2
o>-
1
1
4
6 8 10 12 14
Sessions
Fig. 2
1
4
6 8 10 12 14
Sessions
Fig. 3
Text-fig. 2. Mean number of attacks in each session of eight trials by five octopuses, before
and after removal of the lip. For three sessions before and three after operation the tests were
with crabs, which these octopuses were not allowed to eat (triangles). For the subsequent
eight sessions they were shown a horizontal rectangle and given a piece of fish at every trial,
whether or not they had attacked (circles).
Text-fig. 3. Mean number of attacks at each session of eight trials by a single octopus from
which the lip had been removed. For the first six sessions a horizontal rectangle was shown
and food given (closed circles). For the subsequent six sessions horizontal and vertical
rectangles were shown at alternate trials, food being given with the former and shocks for each
attack at the latter (vertical rectangle, open circles).
Effects of cutting the posterior salivary nerves and
interbuccal connectives
Nerve trunks of four types arise from the front of the superior buccal lobe (Textfig. 1). (1) there are some fifteen labial nerves; (2) at the sides there is a pair of nerves
that run directly to the posterior salivary glands; (3) a pair of interbuccal connectives
join the superior buccal lobe to the inferior buccal ganglion; (4) a pair of cerebrosubradular connectives run close to the interbuccal connectives but by-pass the
inferior buccal ganglion and run direct to the subradular ganglion, which controls
the papilla at the end of the posterior salivary gland duct (Young, 19656).
These bundles of nerves can be reached where they leave the brain by opening the
cranium from above, removing the jelly and extending the incision forwards, if
584
J. Z. YOUNG
necessary until it enters the buccal venous sinus. The labial nerve bundles near to the
mid-line can be cut easily, but it would be difficult to cut those at the sides without
damaging the salivary nerves or the connectives. Conversely, the salivary nerves and
connectives have not been cut without damaging the more lateral labial nerves, but
the more central labial nerves can be left intact after the salivary nerves and connectives have been cut.
In several operations attempts were made to cut the salivary nerves but leave the
connectives, or vice versa. This was successful only in a few animals, which are
sufficient however to establish the functions of the nerves. No attempt has been made
to cut the interbuccal and cerebro-subradular connectives separately.
Table 1. Effects of lesions to the nerves that arise from the superior buccal lobe
(Columns 2 and 3 show the condition of the right and left salivary nerves and interbuccal
and cerebro-subradular connectives ( + , intact; —, completely interrupted; ± , damaged).
Column 4 shows that some labial nerves were damaged in all animals. Column 5 shows
whether the octopus could poison crabs (+ ) or not ( — ) and, similarly, column 6 shows whether
or not it could clean them and column 7 whether it would eat fish. Column 8 shows the number of attacks at the rectangle in each session of five trials, food being offered on every occasion
when it was shown.)
Nerves cut
Octopus
(0
MCN
MCM
MCL
MDQ
MDP
MCX
MDO
MAL
MAM
MAN
MAO
Salivary
<*)
+
+
+
+
+
+
+
±
—
—
Behaviour
Interbuccal
(3)
Labial
nerves
(4)
Poison
crab
(5)
++
+—
++
+—
+—
±
±
±
±
±
±
±
±
±
±
±
+
+
H—
±
+
±
—
_
—
_
_
Clean
crab
(6)
+
+
+
±
+
+
Learning
Eat
fish
(7)
+
+
+
+
+
+
Horizontal + food
(attacks per session)
(8)
5, 5, 5, 5
5,4, 5,4
5,4,5, 5
o, o, o, i, 5, o, 4, 4
i, i, 3 , 4 , 4 , ° , 4, 2
o, 1 , 0 , 2 , 5 , 5
0, o, 0, 1, 0, 0, 3, 1, 1
_
—
—
_
_
—
—
_
1, 0, 0, 0
1, 0, 0, 0
0, 1, 0, 1
1, 1, 0, 0
The operation of opening the buccal sinus and gaining access to the nerves does not
in itself impair the power of the animal to attack, kill and eat crabs, nor to learn to
attack an unfamiliar figure. In several animals the operation had failed to cut the
required trunks and these activities were unimpaired (Table 1). In octopus MCN
there was no damage to the salivary nerves or connectives but all the labial nerves in
the mid-line had been cut, sparing only the labial nerves that run with the connectives
at the side (PI. 1, fig. 1). This animal attacked, killed and cleaned crabs on the day
after operation and later consistently attacked a horizontal rectangle.
In octopus MCM one interbuccal connective was cut and also the labial nerves at
the sides, but the salivary nerves were intact. This animal behaved exactly as the
previous one. In MCL one posterior salivary nerve had been damaged though not
completely cut (PI. 1, figs. 2, 3). On the day after operation it caught crabs but did
not poison them. On the second and subsequent days, however, the crabs were
poisoned and then fully cleaned. The animal responded regularly to the rectangle,
although many of the labial nerves had been cut.
Nervous pathways for poisoning, eating and learning in Octopus
585
In two further animals, MDP and MDQ, one salivary nerve and one interbuccal
connective was left intact (or nearly so). They both showed some imperfections in
killing and eating crabs. MDP only succeeded in poisoning the crab on about half of
the occasions tested, but was able to remove the meat well from those it did kill.
MDQ (PI. 1, fig. 4) poisoned the crabs regularly but sometimes left their carapaces
imperfectly cleaned. Both animals eventually attacked the horizontal rectangle,
although never so regularly as the first three mentioned (Table 1). A normal octopus
leaves the carapace and endophragmal skeleton of the crab quite free of flesh. These
operated animals frequently left some meat in the anterior (enclosed) part of the
carapace and they failed to remove the gills from the endophragmal skeleton (PI. 2,
fig. 9). Moreover, normal octopuses separate the joints of the larger appendages of
the crabs and remove their contents, presumably by suction and/or with the radula.
The operated animals left the appendages unseparated.
Octopus MCX (PI. 1, figs. 5-7) was an animal in which both posterior salivary
nerves were cut and the interbuccal and subradular connectives were cut on one side.
It was unable to poison the crabs but would attack and catch them and could kill
them, apparently by tearing off the carapace. The meat was then removed reasonably
efficiently, though sometimes parts of the skeleton were left uncleaned. This animal
learned to attack the horizontal rectangle when shown. Moreover, it proved to be
able to discriminate between horizontal and vertical rectangles:
Attacks per session
H+
V—
3 5 5 5 5 5
5 1
1 3 0 0
This animal with one interbuccal connective intact could therefore learn, although
it was unable to poison crabs.
In five other octopuses the posterior salivary nerves and interbuccal connectives
were cut on both sides (Table 1). Many of the labial nerves were also cut but some
near the mid-line remained intact (PI. 1, fig. 8). All of these animals attacked crabs
when shown but none was able to poison them. Sometimes the crab was killed, by
pulling it apart, but the meat was never properly removed. These animals did not
eat any of the fish given to them. None of these animals learned to come out to attack
the rectangle.
Octopus MDO was kept alive for 15 days and tested on several occasions by
repeated presentation of crabs at 5 min. intervals. At the beginning of such a session
it would emerge rapidly and seize the crab, but would then drop it and return home.
At later trials of the session it came out more slowly and ultimately failed to attack.
Thus in one session the times taken to attack were 6, 15, 18 sec, no attack, no attack.
When tested again 5 hr. later attacks were made after 4, 20, 5 sec, no attack, 20 sec.
On each occasion when the octopus emerged it swam the whole length of the tank,
touched the crab and returned home without seizing it. Presumably the optic lobe
system was operating to produce an attack but the apparatus for completing the
seizure, killing and swallowing was defective. Accordingly no signals indicating the
results of the attack reached the optic lobes and the tendency to attack crabs became
extinguished.
These results thus give a clear view of the functions of the various nerves involved.
586
J. Z. YOUNG
Innervation of the posterior salivary glands is shown to be necessary for poisoning
but not for learning (octopus MCX). Learning is possible providing that one interbuccal connective is intact (octopuses MDQ and MCX), but not otherwise, even
though some labial nerves are intact (octopus MDO, etc.). Severing most of the
labial nerves does not interfere with learning, but there is no animal in which they
have all been cut without damage to other nerves.
Cutting of cerebro-brackial and buccoal-brachial connectives
This operation was performed on four animals, to test the hypothesis that the act
of poisoning crabs is initiated through one or both of these pathways (PI. 2, figs. 10,
11, octopus NAA) The characteristic syndrome after such an operation was that the
octopus would readily attack and seize crabs but then neither poison nor release
them. The crabs were handled clumsily and the failure to poison them may have been
due to wrong positioning, but probably mainly to absence of the stimulus to eject
the poison in spite of the fact that the posterior salivary nerves were intact (PI. 2,
figs. 10, 11). The animals did sometimes accept fish when given and make one or
more bites in it.
After this operation the suckers are very 'sticky', they do not readily let go. This
phenomenon was noticed by von Uexkull (1895), who called such animals ' Greiftiere'.
The visual response to crabs gradually became extinguished, even though the crabs
were captured. Thus 2 days after the operation octopus MEC made a series of attacks
on crabs, caught and handled them moderately efficiently but never poisoned them.
The crabs were given at 10 min. intervals and attacks were completed in the following times (seconds):
5, 6, 11, 12, 18, 20, no attack.
When the octopus was killed it was found to be carrying a bundle of five live crabs.
There was no damage to the superior buccal lobe and both posterior salivary nerves
were intact throughout. The cerebro-brachial and buccal-brachial connectives were
completely severed on the right side. On the left the inferior frontal-brachial and
posterior buccal-brachial tracts were intact (PI. 2, fig. 12). These are therefore not
the pathways for poisoning, since this was absent in this animal. The superior buccalbrachial tracts were completely cut on the right, and only a few fibres remained on
the left (PI. 2, fig. 13).
It therefore seems that the superior buccal-brachial tracts are necessary for poisoning and for eating even fish meat.
After cutting the cerebro-brachial and buccal-brachial connective on one side only,
an octopus can attack, poison and clean a crab, although sometimes leaving more meat
in the exoskeleton than a normal animal would.
Effects of transections of the brain
These operations were performed after opening the cranium and removing the
jelly. Cuts were usually made with scissors, beginning dorsally and proceeding down
to the level of the dorsal surface of the oesophagus.
In three octopuses (MDI, MCR and MCS) the cut passed down between the
median superior and inferior frontal lobes and behind the posterior buccal lobe
(a)
MDI
n./ab.
'buc.p.
cer.-br.
buc.p.
Fig- 5
Text-fig. 4-5. Tracings from photographs of sagittal sections of lesions in the central nervous
system. The capacity of each animal to poison, eat and learn is shown, a cross indicating that
the capacity in question was absent.
588
J. Z. YOUNG
(Table 2; Text-fig. 40, b). On the day after the operation all three animals attacked
crabs, though one failed to poison them. Subsequently all attacked and poisoned
crabs and cleaned them well. After several days, however, the tendency to attack
crabs declined and then disappeared altogether, presumably because no signals of the
arrival of food were reaching the optic lobes. Through as many as eight sessions each
of five trials with the horizontal rectangle none of these animals came out to attack it.
This was all the more remarkable because they accepted and ate the fish that was
given on each occasion after showing the rectangle. It was noticeable, however, that
they would not come to take the piece of sardine on a wire as normal octopuses do,
but treated it visually as an object to be avoided. Indeed they would often dash
around the tank when it appeared. As soon as the fish touched the arms, however, it
was accepted. Yet even after this long course of positive training the rectangle was
treated as an object to be avoided, the octopus moving away when it approached.
These animals therefore attacked, poisoned and ate crabs and ate fish, but did not
learn to attack a strange figure.
In one animal (octopus LTF) the cut was somewhat farther forward, in front of
the median inferior frontal lobe and passed through the posterior buccal lobe. The
animal attacked, poisoned and ate crabs (Text-fig. 4c). No training with a rectangle
was given.
If the lesion passed through the back or middle of the superior buccal lobe the
animal still attacked crabs seen at a distance but did not poison them (octopuses
MAI, MAK, LZQ, MDN). This can be correlated with obvious degeneration of the
posterior salivary nerve (Text-fig. $a—c). These animals sometimes killed a crab,
apparently by pulling it apart, and they cleaned it, though not always perfectly. The
reflexes for eating are therefore operated through the front part of the superior buccal
lobe. The eating reflexes do not necessarily involve the connective between the
superior buccal and brachial lobes. In octopus MAK this was severed on both sides
but both interbuccal connectives were mainly intact. The octopus did not poison
crabs, but was several times found to have thoroughly cleaned crabs that it had caught
and pulled apart.
These animals with lesions in the superior buccal lobe failed in up to eight sessions
to learn to attack the horizontal rectangle. In the later sessions they frequently refused
to accept the fish offered as food and towards the end of the experiment they refused
also to attack crabs, moving away when the crab approached.
With the transection somewhat further forward the animals did not eat. This
may occur when the cut passes through the centre of the superior buccal lobe (Textfig. 5A) (octopuses, MCY, MCT, LZO), but the exact boundary has not been determined.
In the animals with damage to the superior buccal lobe various abnormalities
appeared. The octopuses often failed to attack crabs from a distance. Even if they
killed and ate them the empty shells were held by the arms for a long time.
If the transection was made through the front of the superior buccal lobe the
animals neither poisoned crabs nor ate them (octopuses MDL and MDM). After
such operations some octopuses seldom attacked crabs when seen at a distance but
others continued to do so. As with all the other transections described the animals
did not learn to attack a rectangle, even if food was given after every presentation
Nervous pathways for poisoning, eating and learning in Octopus
589
for many sessions. Two of these animals had been taught before operation to attack
the horizontal rectangle vigorously and also the vertical one. An attempt was then
made to train the animal (Text-fig. 6) to continue to attack the horizontal (rewarded
with food) but to avoid a vertical rectangle (shocked). At first both shapes were
attacked by this animal but subsequently there were only occasional attacks at one
or the other figure throughout seven sessions of ten trials each. The octopus learned
not to attack the vertical figure, indicating that the pain pathway was intact, but was
unable to continue attacking the horizontal one. After an interval of 2 days the horizontal rectangle was again shown and food given, it was sometimes attacked but these
Cut
2
3
4
5
6
7
8
Sessions
9
10 11
12 13 14
Text-fig. 6. Octopus MDL was trained to attack a horizontal rectangle and then a cut made
through the front of the superior buccal lobes. The mean number of attacks during each subsequent session is shown. For the next seven sessions food was given after each occasion that
the horizontal rectangle was shown (closed circles), for attacks on the vertical rectangle the
animal received a shock (open circles). After a gap of 2 days only the horizontal rectangle was
shown and food given at each trial.
Cut
5|-
V
li
< 3
I
2
I
3 4
I
I
5 6 7
Sessions
Fig. 7
I
I
8
9
10 11
I
I
2
1
3
4
5
I
6
I
7
I
8
I
9
I
10
Sessions
Fig. 8
Text-fig. 7. Mean number of attacks made by four octopuses before and after a cut between
superior and posterior buccal lobes. For the first six sessions tests were with crabs, which the
octopuses were not allowed to eat (triangles). Thereafter a horizontal rectangle was shown and
food given at each trial, though no attacks were made (circles).
Text-fig. 8. Mean number of attacks on a horizontal rectangle by four octopuses before and
after making a cut between superior and posterior buccal lobes. Food was given at every trial,
whether or not there had been an attack. T h e triangle indicates the mean number of attacks
when a crab was shown.
38
Exp. BioL 43, 3
590
J. Z. YOUNG
attacks gradually declined. The other animal (MDM) showed essentially similar
behaviour but with fewer attacks.
These animals therefore show that if a representation has been established in the
visual memory system it can continue to produce its effects even if after operation
signals cannot reach the system from the mouth and gut. However its effectiveness
in producing attacks is not sufficient to allow differentiation between two figures.
The effect of the representation persists for some trials but ultimately undergoes
extinction.
This waning of the effect of a representation established before operation is clearly
shown even for attacks on crabs. The four animals shown in Text-fig. 7 attacked
crabs regularly before operation. Cuts were then made between the superior and
posterior buccal lobes. All the animals continued to attack on the day following
operation, (but none at more than 6/8 trials). On the second day there was a further
fall in attacks by all the animals, with a maximum of 4/8 trials. Tests with the horizontal rectangle and food then failed to produce any attacks in five sessions. These
animals had not of course been trained before operation to attack the rectangle.
A further four octopuses were given food with the rectangle before operation
(Text-fig. 8). Afterwards they attacked more often than the animals not so pretrained, but very irregularly. There was no further learning to attack the rectangle
during seven sessions. At the end of the experiment the animals were tested with
crabs and all attacked at the majority of trials (Text-fig. 8). The failures to attack the
rectangle were therefore not due to ill-health but to the presence before operation
of a 'weak' representation, which could not be reinforced because of severance of
taste pathway.
DISCUSSION
These experiments have shown decisively that the efferent pathways for poisoning
crabs and for cleaning them are distinct. Animals MCX (Table 1) and MAI (Table 2)
were unable to poison, but cleaned the crabs adequately once they had killed them.
Moreover, the results confirm that the nervous pathway to the posterior salivary
glands begins at the back of the superior buccal lobe, a conclusion previously reached
by anatomical methods (Young, 19656). Unfortunately there has been no animal in
which the interbuccal connectives (eating pathway) has been interrupted alone,
leaving the poisoning pathway. This separation clearly cannot be achieved by any
cut within the brain. Neither has the cerebro-subradular connective been cut independently of the other nerves, so it remains uncertain how the control of the salivary
papilla, through the subradular ganglion, is effected.
The discharge of poison is presumably initiated by impulses arriving at the back
of the superior buccal lobe, probably from the arms via the superior buccal-brachial
connective, and the animals in which this connective was cut on both sides were
indeed unable to poison or eat crabs or to eat fish. The ejection of the poison from the
posterior salivary glands is presumably begun before whatever activation there may
be of the salivary papilla, which is probably effected by cells lying more anteriorly
in the superior buccal lobe. It is indeed possible that the operations of the papilla
are largely controlled by reflexes through the subradular ganglion, under little central
control.
Nervous pathways for poisoning, eating and learning in Octopus
591
The pathway by which impulses indicating arrival of food are able to teach the
octopus to attack a given visual shape passes through the interbuccal connectives,
and the superior buccal and posterior buccal lobes. Learning is not possible if there
has been a bilateral interruption anywhere along this course. That this is not due to
general depression as a result of operation is shown by the animals of Table 1, where
the lesions to the salivary nerves or labial nerves do not prevent such learning. There
is no similar control in the operations within the brain, since the pathway was interrupted in all of them (Table 2). However, the animals were all active and many of
them attacked and ate crabs and fish, but yet could not learn.
Table 2. Effects of transections in the front part of the brain
Column 3 shows whether the octopus poisoned crabs ( + ) and column 4 shows whether it
cleaned the exoskeletons ( + ); partial cleaning of the crab is shown as ( ± ). Column 5 shows
whether fish was eaten regularly ( + ), sometimes ( ± ) or never ( —). Column 6 shows the
number of attacks in each session of five trials at a horizontal rectangle, food being given (or
offered) after each occasion that the rectangle was shown.
Learning
Octopus
Level of cut
Poison
Clean
Eat
fish
Horizontal + food
(attacks per sewion)
(1)
(2)
(3)
(4)
(5)
(6)
Behind inf. fr.
MDI
+
o, o, o, o, o, o, o, o
MCR
Behind inf. fr.
+
o, o, o, o, o
MCS
Behind inf. fr.
+
o, o, o, o, o
Behind sup. buc.
LTF
+
No tests
Back sup. buc.
MAI
±
o, o, o, o, o, o
Back sup. buc.
MAK
±
o, o, o, o, o, o
Back sup. buc.
LZQ
+
o, o, o, o
±
Mid. sup. buc.
MDK
±
±
0,1,2,2,0,0,0,0
Mid. sup. buc.
MDN
±
o, o, o, o, o, o, o, o
Mid. sup. buc.
MCY
±
o, o, o, o, o, o, o, o
Mid. sup. buc.
MCT
—
O, O, O, I , O
Mid. sup. buc.
—
o, o, o, o
LZO
The site of the receptors can be approximately identified. They do not lie in the
lips, which can be removed without preventing learning. Neither are they in the
oesophagus. Afferents have been shown to pass from the oesophagus in the sympathetic nerves, but animals with both the nerves cut can learn to attack a rectangle
(Young, unpublished).
The afferent fibres responsible for the learning must therefore lie within the buccal
mass, perhaps in the lateral buccal palps that form the floor of the mouth. Fine
fibres have been seen near the surface of these palps and impulses from them would
pass via the inferior buccal ganglion, and interbuccal connectives, which have been
shown to be the relevant pathway (Young, 19656).
The buccal tract is a bundle of fibres that leaves the interbuccal connective and
passes to the posterior buccal and ultimately to the subvertical lobes (PI. 1, figs. 3, 7;
Text-fig. 4a). This may well be the central course of the fibres. It is not clear whether
they reach the optic lobes direct (via the inferior frontal-optic tract) or through the
inferior frontal-lateral superior frontal tract (perhaps by both routes).
The interruption of this pathway prevents the learning to attack some previously
unfamiliar figure, but after this operation objects that the octopus had previously
learned to attack will still produce a response. However, in all the animals that could
38-2
592
J. Z. YOUNG
not learn, the capacity to attack crabs gradually died away. This is not surprising for
the animals in Table i, since these animals could not eat. However, after section
behind the posterior buccal lobe we find animals that can eat but cannot learn, and in
these also the tendency to attack crabs also died away, presumably by extinction of
the processes that initiate it in the optic lobes if the impulses acting as signals of
results do not reach the lobes.
Octopus LTF with a cut between the superior and posterior buccal lobes was able
to poison and eat crabs efficiently. This gives us the important information that the
posterior buccal lobe is not essential for these processes.
SUMMARY
1. Octopuses after removal of the lip kill and eat crabs apparently normally. They
learn to attack a strange figure moving in the visual field.
2. The pair of nerves that originates from cells at the back of the superior buccal
lobe is shown to be responsible for the discharge of secretion from the posterior salivary glands. If this pair of nerves is interrupted the octopus does not poison a crab
after catching it. It still eats, however, and learns to attack a strange figure.
3. If both interbuccal connectives have been severed the octopus does not remove
the flesh properly from crabs. It does not learn to attack a strange figure.
4. Any operation on the central nervous system that interrupts the pathway from
the interbuccal connectives to the lateral superior frontal and optic lobes prevents
learning to attack a figure that has been seen.
5. If such cuts pass through the middle of the superior buccal lobe the animal
does not poison crabs or completely remove the flesh from their exoskeletons.
6. If the cut is through the back of the superior buccal lobe the octopus does not
poison crabs but may tear them open and then clean and eat them.
7. With cuts still farther back the animal poisons, cleans and eats crabs, but still
does not learn to attack.
I am very grateful to Dr P. Dohrn, the Director, and the staff of the Zoological
Station at Naples for their assistance. Also to Mrs M. Nixon for her help in preparing
the MS for publication. Help with the experiments was also given by Messrs J.
Bendall, M.C. Bishop, E. W. Maclarty, C. J. Mitchell and A. J. Sweatman.
The work has been sponsored in part by the Air Force Office of Scientific Research
under Grant AF EOAR with the European Office.
APPENDIX
Abbreviations
brachial lobe
buc.int.con. interbuccal connective
buc.p.
posterior buccal lobe
buc.p.-br. posterior buccal to brachial connective
buc.t.
superior buccal lobe
buc.s.-br.
superior buccal to brachial connective
c.br.sup.
suprabrachial commissure
br.
c.opt.v.
cer.-br.
duc.tal.p
fr.i.-br.
fr.i.-frj.
fr.U.
fr.i.med.
ventral optic commissure
cerebro-brachial connective
duct of the posterior salivary gland
inferior frontal to brachial connective
inferior frontal to superior frontal
connective
lateral inferior frontal lobe
median inferior frontal lobe
Journal of Experimental Biology, Vol. 43, No. 3
J. Z. YOUNG
Plate 1
(Facing p. 592)
Journal of Experimental Biology, Vol. 43, No. 3
j . z. YOUNG
Plate 2
Nervous pathways for poisoning, eating and learning in Octopus
fr.s.med.
g.tal.p.
gan.buc.i.
gan.subr.
let.
n.lab.
n.lab.cen.
n.lab.cu.
n.lab.per.
n.sal.p.
median superior frontal lobe
posterior salivary gland
inferior buccal ganglion
subradular ganglion
position of lesion
labial nerve
central end of labial nerve
cut labial nerve
peripheral stump of cut labial nerve
posterior salivary nerve
oes.
rod.
rad.pro.
rad.ret.
sal.pap.
su.
sub.fr.
tr.br.-opt.
tr.buc.
V.
593
oesophagus
radula
radula protractor
radula retractor
papilla of the posterior salivary duct
sucker
subfrontal lobe
brachio-optic lobe tract
buccal tract
vertical lobe
REFERENCES
BOYCOTT, B. B. & YOUNG, J. Z. (1955). Memories controlling attacks on food objects by Octopus
vulgaris Lam. Pubbl. Staz. zool. Napoli, 37, 232-49.
GHIRETTI, F. (i960). Toxicity of octopus saliva against Crustacea. Ann. N. Y. Acad. Set. 90, 726-41.
UEXKOLL, J. VON (1895). Physiologische Untersuchungen an Eledone moschata. IV. Zur Analyse der
Funktionen des Centralnervensystems. Z. Biol. 31, 584—609.
YOUNG, J. Z. (1956). Visual responses by octopus to crabs and other figures before and after training.
J. Exp. Biol. 33, 709-29.
YOUNG, J. Z. (1958). Responses of untrained octopuses to various figures and the effect of removal of
the vertical lobe. Proc. Roy. Soc. B, 149, 463-83.
YOUNG, J. Z. (1965 a). Centres for touch discrimination in Octopus vulgaris. Phil. Trans. B, 249,
45-67.
YOUNG, J. Z. (19656). The buccal nervous system of Octopus. Phil. Trans. B, 249, 27-44.
EXPLANATION OF PLATES
PLATE I (all figures of same magnification)
Fig. 1. Horizontal section through top of superior buccal lobe, the labial nerves having been cut 9 days
previously (octopus MCN).
Fig. 2. Sagittal section showing posterior salivary nerve damaged 9 days previously (octopus MCL).
Fig. 3. The opposite side of the animal shown in figure 2; the nerves are undamaged.
Fig. 4. Horizontal section of superior buccal lobe 10 days after the posterior salivary nerve and interbuccal connective had been cut on one side (octopus MDQ).
Fig. 5. Sagittal section showing lesion interrupting the posterior salivary nerve and interbuccal connective (13 days, octopus MCX).
Figs. 6, 7. Sections of the opposite side to that shown in fig. 5. The posterior salivary nerve has been
cut, but the interbuccal connective is intact.
Fig. 8. Horizontal section showing the majority of the labial nerves cut seven days previously, but a
few near the mid-line intact (n. lab.) (octopus MAL).
PLATE 2
Fig. 9 A. Carapace and endophragmal skeleton of a crab as they appear after being cleaned and eaten
by a normal octopus. B. A crab with much meat left after being attacked and taken by an octopus
with the superior buccal lobe damaged.
Figs, io, 11. Sagittal sections from the two sides of octopus NAA in which both cerebro-brachial
connectives were completely cut. The animal could not poison or eat crabs in spite of the fact that
both posterior salivary nerves and interbuccal connectives were intact.
Figs. 12, 13. Transverse sections of octopus MEC in which both buccal-brachial connectives were
damaged but on one side (L) the inferior frontal-brachial and superior buccal-brachial tracts were
intact. Notice degeneration throughout the lateral inferior frontal lobe on right but not left,.